Antimicrobial peptides (AMPs) selectively target and form pores in microbial membranes. We report an experimentally guided unbiased simulation methodology that yields the mechanism of spontaneous pore assembly for the AMP maculatin at atomic resolution. Rather than a single pore, maculatin forms an ensemble of structurally diverse temporarily functional low-oligomeric pores, which mimic integral membrane protein channels in structure. These pores continuously form and dissociate in the membrane. Membrane permeabilization is dominated by hexa-, hepta-, and octomers, which conduct water, ions, and small dyes. Pores formed by consecutive addition of individual helices to a transmembrane helix or helix bundle, in contrast to current poration models. The diversity of the pore architectures – formed by a single sequence – may be a key feature in preventing self-toxicity and could explain why sequence-function relationships in AMPs remain elusive.